Environmental and Microbial Interactions Shape Methane-Oxidizing Bacterial Communities in a Stratified Lake

Guggenheim, Carole; Freimann, Remo; Mayr, Magdalena; Beck, Karin; Wehrli, Bernhard; Bürgmann, Helmut

doi:10.3389/fmicb.2020.579427

Cited by 21 publications

(24 citation statements)

References 117 publications

(151 reference statements)

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“…While we argue that the affinity for CH 4 is a key factor for explaining the niche differentiation between αand -MO, we do not dismiss the importance of other parameters in explaining the distribution and abundance of the genera. It has been shown that at constant CH 4 concentration, O 2 has a selecting effect on -MO communities (Hernandez et al, 2015) and other variables like light, metals, or nitrogen compounds have had both inhibiting or enhancing effects on CH 4 oxidation depending on the conditions (Rudd et al, 1976;Bédard and Knowles, 1989;Murase and Sugimoto, 2005;Milucka et al, 2015;Guggenheim et al, 2020). However, we could not detect any selection effect for any of the available variables.…”

Section: Ch 4 Affinity Might Define the Relation Between α-Mo And -Mocontrasting

confidence: 79%

Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

et al. 2021

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Boreal lakes and ponds produce two-thirds of the total natural methane emissions above the latitude of 50° North. These lake emissions are regulated by methanotrophs which can oxidize up to 99% of the methane produced in the sediments and the water column. Despite their importance, the diversity and distribution of the methanotrophs in lakes are still poorly understood. Here, we used shotgun metagenomic data to explore the diversity and distribution of methanotrophs in 40 oxygen-stratified water bodies in boreal and subarctic areas in Europe and North America. In our data, gammaproteobacterial methanotrophs (order Methylococcales) generally dominated the methanotrophic communities throughout the water columns. A recently discovered lineage of Methylococcales, Candidatus Methylumidiphilus, was present in all the studied water bodies and dominated the methanotrophic community in lakes with a high relative abundance of methanotrophs. Alphaproteobacterial methanotrophs were the second most abundant group of methanotrophs. In the top layer of the lakes, characterized by low CH4 concentration, their abundance could surpass that of the gammaproteobacterial methanotrophs. These results support the theory that the alphaproteobacterial methanotrophs have a high affinity for CH4 and can be considered stress-tolerant strategists. In contrast, the gammaproteobacterial methanotrophs are competitive strategists. In addition, relative abundances of anaerobic methanotrophs, Candidatus Methanoperedenaceae and Candidatus Methylomirabilis, were strongly correlated, suggesting possible co-metabolism. Our data also suggest that these anaerobic methanotrophs could be active even in the oxic layers. In non-metric multidimensional scaling, alpha- and gammaproteobacterial methanotrophs formed separate clusters based on their abundances in the samples, except for the gammaproteobacterial Candidatus Methylumidiphilus, which was separated from these two clusters. This may reflect similarities in the niche and environmental requirements of the different genera within alpha- and gammaproteobacterial methanotrophs. Our study confirms the importance of O2 and CH4 in shaping the methanotrophic communities and suggests that one variable cannot explain the diversity and distribution of the methanotrophs across lakes. Instead, we suggest that the diversity and distribution of freshwater methanotrophs are regulated by lake-specific factors.

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Section: Ch 4 Affinity Might Define the Relation Between α-Mo And -Mocontrasting

confidence: 79%

Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

et al. 2021

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“…Stratification of lakes is a common seasonal phenomenon of the temperate zone, which is dependent on the depth and the surface area of the lake (Gorham & Boyce, 1989). Stratified lakes show warm and oxygen-rich upper water layers, dominated by cyanobacteria and algae, and colder (anoxic) deeper layers, that harbor heterotrophic biomass-degraders and sulfate-reducing bacteria (Diao et al, 2017(Diao et al, , 2018Guggenheim et al, 2020;Vigneron et al, 2021). In between these layers, the metalimnion can be found, which is formed by decreasing light-intensities and oxygen concentrations (microaerophilic), and an increasing pool of reduced sulfur compounds, creating ideal niches for phototrophic sulfur bacteria and chemolithoautotrophic micro-organisms (Bush et al, 2017;Diao et al, 2017Diao et al, , 2018Jorgensen et al, 1979;Morrison et al, 2017;Nyirabuhoro et al, 2020;Savvichev et al, 2018;Vavourakis et al, 2019;Vigneron et al, 2021;Wörner & Pester, 2019;Wu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Large and interacting effects of temperature and nutrient addition on stratified microbial ecosystems in a small, replicated, and liquid‐dominated Winogradsky column approach

et al. 2021

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Aquatic ecosystems are often stratified, with cyanobacteria in oxic layers and phototrophic sulfur bacteria in anoxic zones. Changes in stratification caused by the global environmental change are an ongoing concern. Increasing understanding of how such aerobic and anaerobic microbial communities, and associated abiotic conditions, respond to multifarious environmental changes is an important endeavor in microbial ecology. Insights can come from observational and experimental studies of naturally occurring stratified aquatic ecosystems, theoretical models of ecological processes, and experimental studies of replicated microbial communities in the laboratory. Here, we demonstrate a laboratory‐based approach with small, replicated, and liquid‐dominated Winogradsky columns, with distinct oxic/anoxic strata in a highly replicable manner. Our objective was to apply simultaneous global change scenarios (temperature, nutrient addition) on this micro‐ecosystem to report how the microbial communities (full‐length 16S rRNA gene seq.) and the abiotic conditions (O2, H2S, TOC) of the oxic/anoxic layer responded to these environmental changes. The composition of the strongly stratified microbial communities was greatly affected by temperature and by the interaction of temperature and nutrient addition, demonstrating the need of investigating global change treatments simultaneously. Especially phototrophic sulfur bacteria dominated the water column at higher temperatures and may indicate the presence of alternative stable states. We show that the establishment of such a micro‐ecosystem has the potential to test global change scenarios in stratified eutrophic limnic systems.

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“…microbial interactions, were also very recently shown to affect the structure of methanotrophic communities, which, however, was beyond the scope of this study (Guggenheim et al . 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Vertical stratification patterns of methanotrophs and their genetic controllers in water columns of oxygen-stratified boreal lakes

Rissanen

Saarela

Jäntti

et al. 2020

FEMS Microbiology Ecology

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The vertical structuring of methanotrophic communities and its genetic controllers remain understudied in the water columns of oxygen-stratified lakes. Therefore, we used 16S rRNA gene sequencing to study the vertical stratification patterns of methanotrophs in two boreal lakes, Lake Kuivajärvi and Lake Lovojärvi. Furthermore, metagenomic analyses were performed to assess the genomic characteristics of methanotrophs in Lovojärvi and the previously studied Lake Alinen Mustajärvi. The methanotroph communities were vertically structured along the oxygen gradient. Alphaproteobacterial methanotrophs preferred oxic water layers, while Methylococcales methanotrophs, consisting of putative novel genera and species, thrived, especially at and below the oxic-anoxic interface and showed distinct depth variation patterns, which were not completely predictable by their taxonomic classification. Instead, genomic differences among Methylococcales methanotrophs explained their variable vertical depth patterns. Genes in clusters of orthologous groups (COG) categories L (replication, recombination and repair) and S (function unknown) were relatively high in metagenome-assembled genomes representing Methylococcales clearly thriving below the oxic-anoxic interface, suggesting genetic adaptations for increased stress tolerance enabling living in the hypoxic/anoxic conditions. By contrast, genes in COG category N (cell motility) were relatively high in metagenome-assembled genomes of Methylococcales thriving at the oxic-anoxic interface, which suggests genetic adaptations for increased motility at the vertically fluctuating oxic-anoxic interface.

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Environmental and Microbial Interactions Shape Methane-Oxidizing Bacterial Communities in a Stratified Lake

Cited by 21 publications

References 117 publications

Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

Candidatus Methylumidiphilus Drives Peaks in Methanotrophic Relative Abundance in Stratified Lakes and Ponds Across Northern Landscapes

Large and interacting effects of temperature and nutrient addition on stratified microbial ecosystems in a small, replicated, and liquid‐dominated Winogradsky column approach

Vertical stratification patterns of methanotrophs and their genetic controllers in water columns of oxygen-stratified boreal lakes

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